Mark I. McCormick

Replenishment of fish populations is threatened by ocean acidification

There is increasing concern that ocean acidification, caused by the uptake of additional CO2 at the ocean surface, could affect the functioning of marine ecosystems; however, the mechanisms by which population declines will occur have not been identified, especially for noncalcifying species such as fishes. Here, we use a combination of laboratory and field-based experiments to show that levels of dissolved CO2 predicted to occur in the ocean this century alter the behavior of larval fish and dramatically decrease their survival during recruitment to adult populations. Altered behavior of larvae was detected at 700 ppm CO2, with many individuals becoming attracted to the smell of predators. At 850 ppm CO2, the ability to sense predators was completely impaired. Larvae exposed to elevated CO2 were more active and exhibited riskier behavior in natural coral-reef habitat. As a result, they had 5–9 times higher mortality from predation than current-day controls, with mortality increasing with CO2 concentration. Our results show that additional CO2 absorbed into the ocean will reduce recruitment success and have far-reaching consequences for the sustainability of fish populations.

Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function

A study of two species of coral reef fish demonstrates that the anticipated increase in atmospheric carbon dioxide directly interferes with neurotransmitter function in their larvae, a hitherto unrecognized problem for marine fishes. Predicted future CO2 levels have been found to alter sensory responses and behaviour of marine fishes. Changes include increased boldness and activity, loss of behavioural lateralization, altered auditory preferences and impaired olfactory function1,2,3,4,5. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats1,3. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function2,6. However, the underlying mechanism linking high CO2 to these diverse responses has been unknown. Here we show that abnormal olfactory preferences and loss of behavioural lateralization exhibited by two species of larval coral reef fish exposed to high CO2 can be rapidly and effectively reversed by treatment with an antagonist of the GABA-A receptor. GABA-A is a major neurotransmitter receptor in the vertebrate brain. Thus, our results indicate that high CO2 interferes with neurotransmitter function, a hitherto unrecognized threat to marine populations and ecosystems. Given the ubiquity and conserved function of GABA-A receptors, we predict that rising CO2 levels could cause sensory and behavioural impairment in a wide range of marine species, especially those that tightly control their acid–base balance through regulatory changes in HCO3− and Cl− levels.

The biology, behavior, and ecology of the pelagic, larval stage of coral reef fishes

[Extract] Reef fish biologists are keenly aware that nearly all bony fishes on coral reefs have a pelagic larval phase that is potentially dispersive, and that this has major implications for reef fish populations not only at evolutionary (or biogeographic) scales, but also at ecological (or demographic, including management) scales. The literature is full of statements of how important this type of life history is for reef fishes, and for study and management of them. However, this realization has not been accompanied by a major shift in research effort to studying this pelagic phase, what one might refer to as “prerecruitment” studies. Neither has it led to a widespread view of the pelagic phase as much more than a “black box” that results in open populations and large fluctuations in recruitment. Even attempts to assess the population connectivity that presumably results from larval dispersal typically make simplifying assumptions, either explicitly or implicitly, that portray the larvae as little more than passive tracers of water movement that “go with the flow”, doing nothing much until they bump into a reef by chance and settle at once. Are larvae really as simple and as uninteresting as the assumptions made by this “black box” view of larval biology? We think not. The work reviewed here reveals larvae of coral reef fishes to have remarkably good swimming abilities, good sensory systems that develop early in ontogeny, and sophisticated behavior that is very flexible. Little of this would have been predicted from the much better known larval biology of temperate, non-reef species such as herring, cod, and plaice. We explore some of the reasons for this. The interaction of larval distributions with oceanography is the subject of Chapter 7 in the present volume, and we do not address that subject area. This chapter is not a revision of former work by Leis (1991a), nor does it cover ground already dealt with in reviews of coral reef fish larval biology by Boehlert (1996) and Cowen and Sponaugle (1997). Instead, here the focus is on recent research that examines reef fish larvae as animals interacting with their environment. The emphasis is on a perspective from the pelagic environment toward the demersal reef environment. The larvae have a similar perspective. Other studies take the opposite view, and indirectly examine the pelagic stage from the reef. These utilize information gleaned from otoliths of recruits or from abundance patterns either of settlement stage larvae captured by reef-edge light traps and reef-based nets, or of recruits on the reef (e.g., Dufour and Galzin, 1993; Milicich, 1994; Sponaugle and Cowen, 1994; Thorrold et al., 1994b,c; Robertson et al., 1999). Studies of this sort provide valuable insight, but they are largely beyond the scope of the present review. We review here new information on the pelagic stage, from spawning to settlement, including metamorphosis, but not postsettlement issues.

BEHAVIORALLY INDUCED MATERNAL STRESS IN A FISH INFLUENCES PROGENY QUALITY BY A HORMONAL MECHANISM

The survival and quality of progeny can be strongly influenced by nongenetic effects derived from the physiological condition of the mother during gametogenesis. The influence of maternal condition on the size and quality of larvae at dispersal was examined for the tropical damselfish, Pomacentrus amboinensis, through a series of field studies during 1994. In this species, males guard a demersal nest of eggs contributed to by nearby females. The largest and most dominant female stays near the nest and contributes most to the egg clutches, limiting egg contributions from subordinate females. Maternal effects dramatically influenced the size of larval progeny at hatching, four days after laying. Much of the variability in progeny size was explained by levels of the stress-associated steroid hormone, cortisol, in the female. A field experiment manipulating maternal levels of cortisol found that cortisol levels strongly influenced the morphology and yolk size of larval progeny at hatching. Variation in the density of egg predators and competitors together explained 38% of the observed variance in maternal cortisol levels. These competitors and predatory fish appear to elevate maternal cortisol levels and consequently influence larval morphology through a stress-related response. This study suggests that the behavioral interaction regime of a fish population can determine larval quality and potentially govern a females contri- bution to the next generation.

Experimental test of the effect of maternal hormones on larval quality of a coral reef fish

Abstract Maternal hormones can play an important role in the development of fish larvae. Levels of the stress hormone, cortisol, in females are elevated by social interactions and transferred directly to the yolk of eggs, where they may influence developmental rates. In some vertebrates, prenatal exposure to high levels of testosterone determine early growth rates, social status and reproductive success. The present study examined whether post-fertilization exposure of eggs of the tropical damselfish, Pomacentrus amboinensis (Pomacentridae), to natural levels of cortisol or testosterone directly affects larval morphology at hatching. Maternal and egg levels of cortisol and testosterone varied widely among clutches of eggs from local populations around Lizard Island on the Great Barrier Reef. The morphology of larvae produced by these local fish populations also varied widely and differed significantly among sites (e.g., standard length: 2.6–3.4 mm; yolk sac area: 0.01–0.13 × 10−2 mm2). Laboratory experiments showed that elevated cortisol levels in the egg reduced larval length at hatching, while slight elevations in testosterone increased yolk sac size. The influence of testosterone, and to a smaller extent cortisol, on larval morphology differed among egg clutches. These differences were partly explained by differences in initial egg hormone levels. Morphological changes induced by experimental hormonal regimes encompassed the entire range of variability in body attributes found in field populations. It is unclear whether cortisol influences growth alone or development rate or both. Testosterone appears to influence yolk utilization rates, and has no significant effect on growth, in contrast to its role in later developmental stages. Maternally derived cortisol and testosterone are important in regulating growth, development, and nutritive reserves of the embryo and larvae of this fish species. Factors that influence the maternal levels of cortisol and testosterone may have a major impact on larval mortality schedules and, therefore, on which breeding individuals contribute to the next generation.

Ocean acidification affects prey detection by a predatory reef fish.

Changes in olfactory-mediated behaviour caused by elevated CO2 levels in the ocean could affect recruitment to reef fish populations because larval fish become more vulnerable to predation. However, it is currently unclear how elevated CO2 will impact the other key part of the predator-prey interaction – the predators. We investigated the effects of elevated CO2 and reduced pH on olfactory preferences, activity levels and feeding behaviour of a common coral reef meso-predator, the brown dottyback (Pseudochromis fuscus). Predators were exposed to either current-day CO2 levels or one of two elevated CO2 levels (∼600 µatm or ∼950 µatm) that may occur by 2100 according to climate change predictions. Exposure to elevated CO2 and reduced pH caused a shift from preference to avoidance of the smell of injured prey, with CO2 treated predators spending approximately 20% less time in a water stream containing prey odour compared with controls. Furthermore, activity levels of fish was higher in the high CO2 treatment and feeding activity was lower for fish in the mid CO2 treatment; indicating that future conditions may potentially reduce the ability of the fish to respond rapidly to fluctuations in food availability. Elevated activity levels of predators in the high CO2 treatment, however, may compensate for reduced olfactory ability, as greater movement facilitated visual detection of food. Our findings show that, at least for the species tested to date, both parties in the predator-prey relationship may be affected by ocean acidification. Although impairment of olfactory-mediated behaviour of predators might reduce the risk of predation for larval fishes, the magnitude of the observed effects of elevated CO2 acidification appear to be more dramatic for prey compared to predators. Thus, it is unlikely that the altered behaviour of predators is sufficient to fully compensate for the effects of ocean acidification on prey mortality.

Elevated carbon dioxide affects behavioural lateralization in a coral reef fish

Elevated carbon dioxide (CO2) has recently been shown to affect chemosensory and auditory behaviour, and activity levels of larval reef fishes, increasing their risk of predation. However, the mechanisms underlying these changes are unknown. Behavioural lateralization is an expression of brain functional asymmetries, and thus provides a unique test of the hypothesis that elevated CO2 affects brain function in larval fishes. We tested the effect of near-future CO2 concentrations (880 µatm) on behavioural lateralization in the reef fish, Neopomacentrus azysron. Individuals exposed to current-day or elevated CO2 were observed in a detour test where they made repeated decisions about turning left or right. No preference for right or left turns was observed at the population level. However, individual control fish turned either left or right with greater frequency than expected by chance. Exposure to elevated-CO2 disrupted individual lateralization, with values that were not different from a random expectation. These results provide compelling evidence that elevated CO2 directly affects brain function in larval fishes. Given that lateralization enhances performance in a number of cognitive tasks and anti-predator behaviours, it is possible that a loss of lateralization could increase the vulnerability of larval fishes to predation in a future high-CO2 ocean.

Estimating total abundance of a large temperate-reef fish using visual strip-transects

Total abundance estimates for the large, common, reef fish Cheilodactylus spectabilis (Hutton) were obtained for a marine reserve and adjacent section of coast in north-eastern New Zealand during 1985. Visual strip-transects were used to estimate abundance and size structure in both areas. The accuracy, precision and cost efficiency of five transect sizes (500, 375, 250, 100, 75 m2) were examined over three times per day (dawn, midday and dusk), by simulating transects over mapped C. spectabilis populations. Two transect sizes showed similarly high efficiency. The smaller of the two (20x5 m) was chosen for the survey because of the general advantages attributable to small sampling units. Biases related to strip-transect size are discussed. Preliminary sampling indicated that C. spectabilis was distributed heterogeneously, and that density was habitat-related. An optimal stratified-random design was employed in both locations, to obtain total abundance and size-structure estimates. This reduced the between-habitat source of variability in density. The total number of sampling units used was governed by the time available. The resulting total abundance estimates obtained were 18 338±2 886 (95% confidence limit) for the 5 km marine reserve, compared to 3 987±1 117 for an adjacent, heavily fished 4 km section of coast. When corrected for total area and habitat area sampled, this represented a 2.3-fold difference in abundance. If sampling had been designed to detect an arbitrary 10% difference in abundance within each habitat, an infeasible 440 h of sampling would have been required. Size-frequency distributions of C. spectabilis at the reserve had a larger model size class than distributions from the adjacent area. The data suggest that reserve status is causal in these differing abundance and size structure estimates.

Putting prey and predator into the CO2 equation – qualitative and quantitative effects of ocean acidification on predator–prey interactions

Little is known about the impact of ocean acidification on predator-prey dynamics. Herein, we examined the effect of carbon dioxide (CO(2)) on both prey and predator by letting one predatory reef fish interact for 24 h with eight small or large juvenile damselfishes from four congeneric species. Both prey and predator were exposed to control or elevated levels of CO(2). Mortality rate and predator selectivity were compared across CO(2) treatments, prey size and species. Small juveniles of all species sustained greater mortality at high CO(2) levels, while large recruits were not affected. For large prey, the pattern of prey selectivity by predators was reversed under elevated CO(2). Our results demonstrate both quantitative and qualitative consumptive effects of CO(2) on small and larger damselfish recruits respectively, resulting from CO(2)-induced behavioural changes likely mediated by impaired neurological function. This study highlights the complexity of predicting the effects of climate change on coral reef ecosystems.

Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity

When unfolded proteins accumulate in the endoplasmic reticulum (ER), the unfolded protein response is activated. This ER stress response restores ER homeostasis by coordinating processes that decrease translation, degrade misfolded proteins, and increase the levels of ER-resident chaperones. Ribonuclease inositol-requiring protein–1 (IRE-1), an endoribonuclease that mediates unconventional splicing, and its target, the XBP-1 transcription factor, are key mediators of the unfolded protein response. In this study, we show that in Caenorhabditis elegans insulin/IGF-1 pathway mutants, IRE-1 and XBP-1 promote lifespan extension and enhance resistance to ER stress. We show that these effects are not achieved simply by increasing the level of spliced xbp-1 mRNA and expression of XBP-1’s normal target genes. Instead, in insulin/IGF-1 pathway mutants, XBP-1 collaborates with DAF-16, a FOXO-transcription factor that is activated in these mutants, to enhance ER stress resistance and to activate new genes that promote longevity.